Effects of Reversible Inactivation of the Primate Mesencephalic Reticular Formation. II. Hypometric Vertical Saccades

2000 ◽  
Vol 83 (4) ◽  
pp. 2285-2299 ◽  
Author(s):  
David M. Waitzman ◽  
Valentine L. Silakov ◽  
Stacy DePalma-Bowles ◽  
Amanda S. Ayers
Keyword(s):  
Reticular Formation ◽  
Main Sequence ◽  
Mesencephalic Reticular Formation ◽  
Medial Longitudinal Fasciculus ◽  
Saccade Amplitude ◽  
Burst Neurons ◽  
Vertical Saccades ◽  
Vertical Saccade ◽  
Omnipause Neurons ◽  
Saccade Duration

Electrical microstimulation and single-unit recording have suggested that a group of long-lead burst neurons (LLBNs) in the mesencephalic reticular formation (MRF) just lateral to the interstitial nucleus of Cajal (INC) (the peri-INC MRF, piMRF) may play a role in the generation of vertical rapid eye movements. Inactivation of this region with muscimol (a GABAA agonist) rapidly produced vertical saccade hypometria (6 injections). In three of six injections, there was a marked reduction in the velocity of vertical saccades out of proportion to saccade amplitude (i.e., saccades fell below the main sequence). This was associated with a moderate increase in saccade duration. Inadvertent inactivation of the INC could not account for these observations because vertical, postsaccadic drift was not observed. Similarly, pure downward saccade hypometria, the hallmark of rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) inactivation, was always preceded by loss of upward saccades in our experiments. We also found a downward and ipsiversive displacement of initial eye position and evidence of a contraversive head tilt following piMRF injections. Saccade latency was shorter after two of six injections. Simulation of a local feedback model provided three possible explanations for vertical saccade hypometria: 1) a shift in the input to the model to request smaller saccades, 2) a reduction of LLBN input to the vertical saccade medium lead burst neurons (MLBNs), or 3) an increase in the gain of the feedback pathway. However, when the second hypothesis was coupled to a shortened duration of the saccade trigger (i.e., the discharge of the omnipause neurons), the physiological observations of piMRF inactivation could be replicated. This suggested that muscimol had targeted structures that provided both long-lead burst activity to the MLBNs in the riMLF and were critical for reactivation of the omnipause neurons. Evidence of markedly reduced vertical saccade amplitude, curved saccade trajectories, increased saccade duration, and saccades that fall below the amplitude/velocity main sequence in these monkeys closely parallels the oculomotor findings of patients with progressive supranuclear palsy (PSP).

Activity of Mesencephalic Vertical Burst Neurons During Saccades and Smooth Pursuit

2000 ◽  
Vol 83 (4) ◽  
pp. 2080-2092 ◽  
Author(s):  
M. Missal ◽  
S. de Brouwer ◽  
P. Lefèvre ◽  
E. Olivier
Keyword(s):  
Vertical Velocity ◽  
Smooth Pursuit ◽  
Medial Longitudinal Fasciculus ◽  
Eye Position ◽  
Interstitial Nucleus Of Cajal ◽  
Burst Neurons ◽  
Preferred Direction ◽  
Saccade Onset ◽  
Vertical Saccades ◽  
Eye Velocity

The activity of vertical burst neurons (BNs) was recorded in the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF-BNs) and in the interstitial nucleus of Cajal (NIC-BNs) in head-restrained cats while performing saccades or smooth pursuit. BNs emitted a high-frequency burst of action potentials before and during vertical saccades. On average, these bursts led saccade onset by 14 ± 4 ms (mean ± SD, n = 23), and this value was in the range of latencies (∼5–15 ms) of medium-lead burst neurons (MLBNs). All NIC-BNs ( n = 15) had a downward preferred direction, whereas riMLF-BNs showed either a downward ( n = 3) or an upward ( n = 5) preferred direction. We found significant correlations between saccade and burst parameters in all BNs: vertical amplitude was correlated with the number of spikes, maximum vertical velocity with maximum of the spike density, and saccade duration with burst duration. A correlation was also found between instantaneous vertical velocity and neuronal activity during saccades. During fixation, all riMLF-BNs and ∼50% of NIC-BNs (7/15) were silent. Among NIC-BNs active during fixation (8/15), only two cells had an activity correlated with the eye position in the orbit. During smooth pursuit, most riMLF-BNs were silent (7/8), but all NIC-BNs showed an activity that was significantly correlated with the eye velocity. This activity was unaltered during temporary disappearance of the visual target, demonstrating that it was not visual in origin. For a given neuron, its on-direction during smooth pursuit and saccades remained identical. The activity of NIC-BNs during both saccades and smooth pursuit can be described by a nonlinear exponential function using the velocity of the eye as independent variable. We suggest that riMLF-BNs, which were not active during smooth pursuit, are vertical MLBNs responsible for the generation of vertical saccades. Because NIC-BNs discharged during both saccades and pursuit, they cannot be regarded as MLBNs as usually defined. NIC-BNs could, however, be the site of convergence of both the saccadic and smooth pursuit signals at the premotoneuronal level. Alternatively, NIC-BNs could participate in the integration of eye velocity to eye position signals and represent input neurons to a common integrator.

Response Properties of Saccade-Related Burst Neurons in the Central Mesencephalic Reticular Formation

1997 ◽  
Vol 78 (4) ◽  
pp. 2164-2175 ◽  
Author(s):  
Ari Handel ◽  
Paul W. Glimcher
Keyword(s):  
Reticular Formation ◽  
Light Emitting Diode ◽  
Low Frequency ◽  
Mesencephalic Reticular Formation ◽  
Restricted Range ◽  
Response Properties ◽  
Burst Neurons ◽  
Central Mesencephalic Reticular Formation ◽  
Saccadic Target ◽  
Behaving Monkeys

Handel, Ari and Paul W. Glimcher. Response properties of saccade-related burst neurons in the central mesencephalic reticular formation. J. Neurophysiol. 78: 2164–2175, 1997. We studied the activity of saccade-related burst neurons in the central mesencephalic reticular formation (cMRF) in awake behaving monkeys. In experiment 1, we examined the activity of single neurons while monkeys performed an average of 225 delayed saccade trials that evoked gaze shifts having horizontal and vertical amplitudes between 2 and 20°. All neurons studied generated high-frequency bursts of activity during some of these saccades. For each neuron, the duration and frequency of these bursts of activity reached maximal values when the monkey made movements within a restricted range of horizontal and vertical amplitudes. The onset of the movement followed the onset of the burst by the longest intervals for movements within a restricted range of horizontal and vertical amplitudes. The range of movements for which this interval was longest varied from neuron to neuron. Across the population, these ranges included nearly all contraversive saccades with horizontal and vertical amplitudes between 2 and 20°. In experiment 2, we used the following task to examine the low-frequency prelude of activity that cMRF neurons generate before bursting: the monkey was required to fixate a light-emitting diode (LED) while two eccentric visual stimuli were presented. After a delay, the color of the fixation LED was changed, identifying one of the two eccentric stimuli as the saccadic target. After a final unpredictable delay, the fixation LED was extinguished and the monkey was reinforced for redirecting gaze to the identified saccadic target. Some cMRF neurons fired at a low frequency during the interval after the fixation LED changed color but before it was extinguished. For many neurons, the firing rate during this interval was related to the metrics of the movement the monkey made at the end of the trial and, to a lesser degree, to the location of the eccentric stimulus to which a movement was not directed.

Structure of the primate oculomotor burst generator. I. Medium-lead burst neurons with upward on-directions

1991 ◽  
Vol 65 (2) ◽  
pp. 203-217 ◽  
Author(s):  
A. K. Moschovakis ◽  
C. A. Scudder ◽  
S. M. Highstein
Keyword(s):  
Eye Movements ◽  
Mesencephalic Reticular Formation ◽  
Medial Longitudinal Fasciculus ◽  
Posterior Commissure ◽  
Inferior Rectus ◽  
Interstitial Nucleus Of Cajal ◽  
Burst Neurons ◽  
Physiological Characterization ◽  
Highly Correlated ◽  
Oculomotor Complex

1. To investigate the structure of the primate burst generator for vertical saccades, we obtained intra-axonal records from vertical medium-lead burst neurons with upward on-directions (UMLBs) in alert, behaving squirrel monkeys, while monitoring their spontaneous eye movements. After physiological characterization, these UMLBs were injected with horseradish peroxidase. 2. UMLBs (n = 14) had no spontaneous activity and emitted bursts of action potentials that preceded rapid eye movements by approximately 6 ms. Parameters of the burst (duration and number of spikes) were highly correlated with parameters of the rapid eye movement (duration and amplitude of the upward displacement of the eyes). 3. The axons of six UMLBs projected to the oculomotor complex. Their somata (4 were recovered) were all in the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF). Their axons traveled caudally in the medial longitudinal fasciculus (MLF) and ramified in the interstitial nucleus of Cajal (NIC) before entering the oculomotor nucleus. Five axons terminated bilaterally in the subdivisions innervating the superior rectus and inferior oblique muscles and therefore were presumed to be excitatory. One axon terminated in the ipsilateral inferior rectus and superior oblique subdivisions of the oculomotor complex and was presumed to be inhibitory. 4. Additionally, our data demonstrate that the nucleus of the posterior commissure (nPC) may also contain UMLBs. The axon of one such neuron crossed the midline within the posterior commissure and provided terminal fields to the contralateral nPC, riMLF, NIC, and the mesencephalic reticular formation but not to the oculomotor complex. 5. In conclusion, our data demonstrate that the rostral mesencephalon of the monkey contains neurons that have both the activity and the connections that are necessary either to provide motoneurons innervating extraocular muscles of both eyes with the pulse of activity they display during upward saccades or to inhibit their antagonists. Furthermore, our data demonstrate that some UMLBs are better suited for closing the feedback path of the local feedback loop rather than for providing direct input to extraocular motoneurons.

Effects of Reversible Inactivation of the Primate Mesencephalic Reticular Formation. I. Hypermetric Goal-Directed Saccades

2000 ◽  
Vol 83 (4) ◽  
pp. 2260-2284 ◽  
Author(s):  
David M. Waitzman ◽  
Valentine L. Silakov ◽  
Stacy DePalma-Bowles ◽  
Amanda S. Ayers
Keyword(s):  
Reticular Formation ◽  
Single Neuron ◽  
Head Tilt ◽  
Mesencephalic Reticular Formation ◽  
Initial Position ◽  
Oculomotor Control ◽  
Saccade Amplitude ◽  
Reversible Inactivation ◽  
Velocity Signal ◽  
Square Wave

Single-neuron recording and electrical microstimulation suggest three roles for the mesencephalic reticular formation (MRF) in oculomotor control: 1) saccade triggering, 2) computation of the horizontal component of saccade amplitude (a feed-forward function), and 3) feedback of an eye velocity signal from the paramedian zone of the pontine reticular formation (PPRF) to higher structures. These ideas were tested using reversible inactivation of the MRF with pressure microinjection of muscimol, a GABAA agonist, in four rhesus monkeys prepared for chronic single-neuron and eye movement recording. Reversible inactivation revealed two subregions of the MRF: ventral-caudal and rostral. The ventral-caudal region, which corresponds to the central MRF, the cMRF, or nucleus subcuneiformis, is the focus of this paper and is located lateral to the oculomotor nucleus and caudal to the posterior commissure (PC). Inactivation of the cMRF produced contraversive, upward saccade hypermetria. In three of eight injections, the velocity of hypermetric saccades was too fast for a given saccade amplitude, and saccade duration was shorter. The latency for initiation of most contraversive saccades was markedly reduced. Fixation was also destabilized with the development of macrosaccadic square-wave jerks that were directed toward a contraversive goal in the hypermetric direction. Spontaneous saccades collected in total darkness were also directed toward the same orbital goal, up and to the contraversive side. Three of eight muscimol injections were associated with a shift in the initial position of the eyes. A contralateral head tilt was also observed in 5 out of 8 caudal injections. All ventral-caudal injections with head tilt showed no evidence of vertical postsaccadic drift. This suggested that the observed changes in head movement and posture resulted from inactivation of the caudal MRF and not spread of the muscimol to the interstitial nucleus of Cajal (INC). Evidence of hypermetria strongly supports the idea that the ventral-caudal MRF participates in the feedback control of saccade accuracy. However, development of goal-directed eye movements, as well as a shift in the initial position following some of the cMRF injections, suggest that this region also contributes to the generation of an estimate of target or eye position coded in craniotopic coordinates. Last, the observed reduction in contraversive saccade latency and development of macrosaccadic square-wave jerks supports a role of the MRF in saccade triggering.

Effects of Voluntary Blinks on Saccades, Vergence Eye Movements, and Saccade-Vergence Interactions in Humans

2002 ◽  
Vol 88 (3) ◽  
pp. 1220-1233 ◽  
Author(s):  
H. Rambold ◽  
A. Sprenger ◽  
C. Helmchen
Keyword(s):  
Eye Movements ◽  
Peak Velocity ◽  
Saccade Onset ◽  
Vertical Saccades ◽  
Acceleration And Deceleration ◽  
Tightly Coupled ◽  
Measured Effect ◽  
Straight Ahead ◽  
Omnipause Neurons ◽  
Saccade Duration

Blinks are known to change the kinematic properties of horizontal saccades, probably by influencing the saccadic premotor circuit. The neuronal basis of this effect could be explained by changes in the activity of omnipause neurons in the nucleus raphe interpositus or in the saccade-related burst neurons of the superior colliculus. Omnipause neurons cease discharge during both saccades and vergence movements. Because eyelid blinks can influence both sets of neurons, we hypothesized that blinks would influence the kinematic parameters of saccades in all directions, vergence, and saccade-vergence interactions. To test this hypothesis, we investigated binocular eye and lid movements in five normal healthy subjects with the magnetic search coil technique. The subjects performed conjugate horizontal and vertical saccades from gaze straight ahead to targets at 20° up, down, right, or left while either attempting not to blink or voluntarily blinking. While following the same blink instruction, subjects made horizontal vergence eye movements of 7° and combined saccade-vergence movements with a version amplitude of 20°. The movements were performed back and forth from two targets simultaneously presented nearby (38 cm) and more distant (145 cm). Small vertical saccades accompanied most vergence movements. These results show that blinks change the kinematics (saccade duration, peak velocity, peak acceleration, peak deceleration) of not only horizontal but also of vertical saccades, of horizontal vergence eye movements, and of combined saccade-vergence eye movements. Peak velocity, acceleration, and deceleration of eye movements were decreased on the average by 30%, and their duration increased by 43% on the average when they were accompanied by blinks. The blink effect was time dependent with respect to saccade and vergence onset: the greatest effect occurred 100 ms prior to saccade onset, whereas there was no effect when the blink started after saccade onset. The effects of blinks on saccades and vergence, which are tightly coupled to latency, support the hypothesis that blinks cause profound spatiotemporal perturbations of the eye movements by interfering with the normal saccade/vergence premotor circuits. However, the measured effect may to a certain degree but not exclusively be explained by mechanical interference.

scholarly journals Coupling Between Horizontal and Vertical Components of Saccadic Eye Movements During Constant Amplitude and Direction Gaze Shifts in the Rhesus Monkey

2008 ◽  
Vol 100 (6) ◽  
pp. 3375-3393 ◽  
Author(s):  
Edward G. Freedman
Keyword(s):  
Eye Movements ◽  
Saccadic Eye Movements ◽  
Head Movements ◽  
Horizontal Meridian ◽  
Constant Amplitude ◽  
Saccade Amplitude ◽  
Gaze Shifts ◽  
Horizontal Saccade ◽  
Vertical Saccade ◽  
Saccade Duration

When the head is free to move, changes in the direction of the line of sight (gaze shifts) can be accomplished using coordinated movements of the eyes and head. During repeated gaze shifts between the same two targets, the amplitudes of the saccadic eye movements and movements of the head vary inversely as a function of the starting positions of the eyes in the orbits. In addition, as head-movement amplitudes and velocities increase, saccade velocities decline. Taken together these observations lead to a reversal in the expected correlation between saccade duration and amplitude: small-amplitude saccades associated with large head movements can have longer durations than larger-amplitude saccades associated with small head movements. The data in this report indicate that this reversal occurs during gaze shifts along the horizontal meridian and also when considering the horizontal component of oblique saccades made when the eyes begin deviated only along the horizontal meridian. Under these conditions, it is possible to determine whether the variability in the duration of the constant amplitude vertical component of oblique saccades is accounted for better by increases in horizontal saccade amplitude or increases in horizontal saccade duration. Results show that vertical saccade duration can be inversely related to horizontal saccade amplitude (or unrelated to it) but that horizontal saccade duration is an excellent predictor of vertical saccade duration. Modifications to existing hypotheses of gaze control are assessed based on these new observations and a mechanism is proposed that can account for these data.

Structure-function relationships in the primate superior colliculus. II. Morphological identity of presaccadic neurons

1988 ◽  
Vol 60 (1) ◽  
pp. 263-302 ◽  
Author(s):  
A. K. Moschovakis ◽  
A. B. Karabelas ◽  
S. M. Highstein
Keyword(s):  
Superior Colliculus ◽  
Reticular Formation ◽  
Preceding Paper ◽  
Mesencephalic Reticular Formation ◽  
Burst Neurons ◽  
Cells Of Origin ◽  
Efferent Neurons ◽  
Tectal Neurons ◽  
Recurrent Collaterals ◽  
Morphological Identity

1. Microelectrodes filled with horseradish peroxidase (HRP) were inserted in the superior colliculus (SC) of alert squirrel monkeys. Spontaneous eye movements were monitored in the dark during recording and intraaxonal injection of fibers carrying presaccadic signals. 2. Analysis of the relationship between neuronal activity and saccadic parameters indicates that saccade-related neurons can be functionally classified into: 1) vectorial long-lead burst neurons (n = 31), and 2) directional long-lead burst neurons. 3. Vectorial long-lead burst neurons have little if any spontaneous activity and burst intensely before spontaneous saccades within their movement fields with a latency of approximately 20 ms. Their cell bodies were recovered mostly (4/5) in the stratum opticum of the SC. The mediolateral and anteroposterior location of these tectal long-lead burst neurons (TLLBs) together with their movement fields are consistent with existing descriptions of the motor map of the deeper tectal layers. Due to their somatodendritic morphology and pattern of axonal trajectories, TLLBs belong to the T group of tectal efferent neurons that was described in our companion report. Through its branched axonal system each TLLB can relay a signal coding intended eye displacement to reticular targets of the predorsal bundle (PDB), contralateral tectum, ipsilateral mesencephalic reticular formation (MRF), and rostrally located ipsilateral targets of the SC, besides participating in intratectal information processing. 4. Recovered tectal neurons (n = 4) with activity not related to spontaneous saccades participate in the predorsal and ventral ascending tectofugal bundles as well as the projection to the ipsilateral mesencephalic reticular formation. They do not participate in the commissural projection of the SC and need not have recurrent collaterals. Due to their somatodendritic morphology and pattern of axonal trajectories, these cells belong to the X group of tectal efferent neurons that was described in the preceding paper. 5. Recovered cells of origin of directional long-lead burst fibers recorded in the SC (n = 5) are located in the tectorecipient portion of the MRF and their axonal terminals are entirely contained within the SC. The high-frequency portion of the discharge of these reticulotectal long-lead burst neurons (RTLLBs) precedes most contraversive saccades by approximately 19 ms.(ABSTRACT TRUNCATED AT 400 WORDS)

Direct inhibitory synaptic connections of pontine omnipause neurons with burst neurons in Forel's field H related to vertical saccades in the cat

1989 ◽  
Vol 104 (1-2) ◽  
pp. 77-82 ◽  
Author(s):  
Shozo Nakao ◽  
Yoshimitsu Shiraishi ◽  
Masumi Inagaki ◽  
Shigeru Adachi ◽  
Hirohisa Oda ◽  
...  
Keyword(s):  
Synaptic Connections ◽  
Burst Neurons ◽  
Vertical Saccades ◽  
Forel's Field H ◽  
Omnipause Neurons

Anatomy and physiology of the primate interstitial nucleus of Cajal I. efferent projections

1996 ◽  
Vol 75 (2) ◽  
pp. 725-739 ◽  
Author(s):  
T. Kokkoroyannis ◽  
C. A. Scudder ◽  
C. D. Balaban ◽  
S. M. Highstein ◽  
A. K. Moschovakis
Keyword(s):  
Superior Colliculus ◽  
Reticular Formation ◽  
Mesencephalic Reticular Formation ◽  
Head Movements ◽  
Zona Incerta ◽  
Medial Longitudinal Fasciculus ◽  
Thalamic Nuclei ◽  
Posterior Commissure ◽  
Interstitial Nucleus Of Cajal ◽  
Efferent Projections

1. The efferent projections of the interstitial nucleus of Cajal (NIC) were studied in the squirrel monkey after iontophoretic injections of biocytin and Phaseolus Vulgaris leucoagglutinin into the NIC. To ensure the proper placement of the tracer, the same pipettes were used to extracellularly record the discharge pattern of NIC neurons. 2. Three projection systems of the NIC were distinguished: commissural (through the posterior commissure), descending, and ascending. 3. The posterior commissure system gave rise to dense terminal fields in the contralateral NIC, the oculomotor nucleus, and the trochlear nucleus. 4. The descending system of NIC projections deployed dense terminal fields in the ipsilateral gigantocellular reticular formation and the paramedian reticular formation of the pons, as well as in the ventromedial and commissural nuclei of the first two spinal cervical segments. It also gave rise to moderate or weak terminal fields in the vestibular complex, the nucleus prepositus hypoglossi, the inferior olive, and the magnocellular reticular formation, as well as cell groups scattered along the paramedian tracts in the pons and the pontine and medullary raphe. 5. The ascending system of NIC projections gave rise to dense terminal fields in the ipsilateral mesencephalic reticular formation and the zona incerta as well as moderate or weak terminal fields in the ipsilateral centromedian and parafascicular thalamic nuclei. It also provided dense bilateral labeling of the rostral interstitial nucleus of the medial longitudinal fasciculus and the fields of Forel, and moderate or weak bilateral labeling of the mediodorsal, central medial, and central lateral nuclei of the thalamus. 6. Models of saccade generation that rely on feedback from the velocity-to-position integrators and include the superior colliculus in their local feedback loop are contradicted because no fibers originating from the NIC traveled to the superior colliculus to deploy terminal fields. 7. Consistent with its morphological and functional diversity, these data indicate that the primate NIC sends signals to a multitude of targets implicated in the control of eye and head movements.

Sign in / Sign up

Export Citation Format

Share Document